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      Upper ocean oxygenation, evolution of RuBisCO and the Phanerozoic succession of phytoplankton

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      Free Radical Biology & Medicine
      Elsevier Science

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          Abstract

          Evidence is compiled to demonstrate a redox scale within Earth's photosynthesisers that correlates the specificity of their RuBisCO with organismal metabolic tolerance to anoxia, and ecological selection by dissolved O 2/CO 2 and nutrients. The Form 1B RuBisCO found in the chlorophyte green algae, has a poor selectivity between the two dissolved substrates, O 2 and CO 2, at the active site. This enzyme appears adapted to lower O 2/CO 2 ratios, or more “anoxic” conditions and therefore requires additional energetic or nutrient investment in a carbon concentrating mechanism (CCM) to boost the intracellular CO 2/O 2 ratio and maintain competitive carboxylation rates under increasingly high O 2/CO 2 conditions in the environment. By contrast the coccolithophores and diatoms evolved containing the more selective Rhodophyte Form 1D RuBisCO, better adapted to a higher O 2/CO 2 ratio, or more oxic conditions. This Form 1D RuBisCO requires lesser energetic or nutrient investment in a CCM to attain high carboxylation rates under environmentally high O 2/CO 2 ratios. Such a physiological relationship may underpin the succession of phytoplankton in the Phanerozoic oceans: the coccolithophores and diatoms took over the oceanic realm from the incumbent cyanobacteria and green algae when the upper ocean became persistently oxygenated, alkaline and more oligotrophic. The facultatively anaerobic green algae, able to tolerate the anoxic conditions of the water column and a periodically inundated soil, were better poised to adapt to the fluctuating anoxia associated with periods of submergence and emergence and transition onto the land. The induction of a CCM may exert a natural limit to the improvement of RuBisCO efficiency over Earth history. Rubisco specificity appears to adapt on the timescale of ∼100 Myrs. So persistent elevation of CO 2/O 2 ratios in the intracellular environment around the enzyme, may induce a relaxation in RuBisCO selectivity for CO 2 relative to O 2. The most efficient RuBisCO for net carboxylation is likely to be found in CCM-lacking algae that have been exposed to hyperoxic conditions for at least 100 Myrs, such as intertidal brown seaweeds.

          Graphical abstract

          Highlights

          • Dissolved O 2/CO 2 selects for a redox scale of phytoplankton Rubisco substrate selectivity and anaerobic metabolic ability.

          • Increasing O 2/CO 2 induced a positive feedback selecting for red-algal derived plastids at the start of the Mesozoic.

          • The relative affinity of RuBisCO for O 2 and CO 2 tunes to compensate for environmental O 2/CO 2 on timescales of 100–1000 yrs.

          • Induction of a CCM relaxes enzyme specificity over ∼ 100 Myrs providing a limit to improvement of RuBisCO selectivity.

          • Persistently high O 2/CO 2 ratios in restricted intertidal zones selects the most efficient RuBisCO in species lacking a CCM.

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          Most cited references90

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          Carbon dioxide in water and seawater: the solubility of a non-ideal gas

          R.F. Weiss (1974)
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            High-resolution carbon dioxide concentration record 650,000-800,000 years before present.

            Changes in past atmospheric carbon dioxide concentrations can be determined by measuring the composition of air trapped in ice cores from Antarctica. So far, the Antarctic Vostok and EPICA Dome C ice cores have provided a composite record of atmospheric carbon dioxide levels over the past 650,000 years. Here we present results of the lowest 200 m of the Dome C ice core, extending the record of atmospheric carbon dioxide concentration by two complete glacial cycles to 800,000 yr before present. From previously published data and the present work, we find that atmospheric carbon dioxide is strongly correlated with Antarctic temperature throughout eight glacial cycles but with significantly lower concentrations between 650,000 and 750,000 yr before present. Carbon dioxide levels are below 180 parts per million by volume (p.p.m.v.) for a period of 3,000 yr during Marine Isotope Stage 16, possibly reflecting more pronounced oceanic carbon storage. We report the lowest carbon dioxide concentration measured in an ice core, which extends the pre-industrial range of carbon dioxide concentrations during the late Quaternary by about 10 p.p.m.v. to 172-300 p.p.m.v.
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              CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution.

              The evolution of organisms capable of oxygenic photosynthesis paralleled a long-term reduction in atmospheric CO2 and the increase in O2. Consequently, the competition between O2 and CO2 for the active sites of RUBISCO became more and more restrictive to the rate of photosynthesis. In coping with this situation, many algae and some higher plants acquired mechanisms that use energy to increase the CO2 concentrations (CO2 concentrating mechanisms, CCMs) in the proximity of RUBISCO. A number of CCM variants are now found among the different groups of algae. Modulating the CCMs may be crucial in the energetic and nutritional budgets of a cell, and a multitude of environmental factors can exert regulatory effects on the expression of the CCM components. We discuss the diversity of CCMs, their evolutionary origins, and the role of the environment in CCM modulation.
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                Author and article information

                Contributors
                Journal
                Free Radic Biol Med
                Free Radic. Biol. Med
                Free Radical Biology & Medicine
                Elsevier Science
                0891-5849
                1873-4596
                20 August 2019
                20 August 2019
                : 140
                : 295-304
                Affiliations
                [1]Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, OX1 3AN, UK
                Author notes
                []Corresponding author. rosr@ 123456earth.ox.ac.uk
                Article
                S0891-5849(18)32466-3
                10.1016/j.freeradbiomed.2019.05.006
                6856715
                31075497
                ac9d4a3f-bfee-4768-964a-3d2b2ac62ed8
                © 2019 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                Categories
                Article

                Molecular biology
                Molecular biology

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